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Isolation and Chemical Characterization of Pwtx-II: a Novel Alkaloid Toxin from the Venom of the Spider Parawixia Bistriata (Araneidae, Araneae)

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Isolation and Chemical Characterization of Pwtx-II: a Novel Alkaloid Toxin from the Venom of the Spider Parawixia Bistriata (Araneidae, Araneae) Toxicon 46 (2005) 786–796 www.elsevier.com/locate/toxicon Isolation and chemical characterization of PwTx-II: A novel alkaloid toxin from the venom of the spider Parawixia bistriata (Araneidae, Araneae) Lilian M.M. Cesara, Maria A. Mendesa, Claudio F. Tormenab, Maurı´cio R. Marquesa, Bibiana M. de Souzaa, Daniel Menezes Saidemberga, Jackson C. Bittencourtc, Mario S. Palmaa,* aInstitute of Biosciences, Sa˜o Paulo State University (UNESP), Avenue 24 A, 1515-Bela vista, 13506-900 Rio Claro, SP, Brazil bDepartment of Chemistry, Faculdade de Filosofia Cieˆncias e Letras da Universidade de Sa˜o Paulo, FFCLRP-USP, Av. Bandeirantes, 3900, 14040-901 Ribeira˜o Preto, SP, Brazil cLaboratory of Chemical Neuroanatomy, Department of Anatomy, Institute of Biomedical Sciences, University of Sa˜o Paulo (USP), Sa˜o Paulo 05508-900, Brazil Received 9 June 2005; revised 10 August 2005; accepted 11 August 2005 Available online 23 September 2005 Abstract Brazil has many species of spiders belonging to Araneidae family however, very little is known about the composition, chemical structure and mechanisms of action of the main venom components of these spiders. The main objective of this work was to isolate and to perform the chemical characterization of a novel b-carboline toxin from the venom of the spider Parawixia bistriata, a typical species of the Brazilian ‘cerrado’. The toxin was purified by RP-HPLC and structurally elucidated by using a combination of different spectroscopic techniques (UV, ESI-MS/MS and 1H NMR), which permitted the assignment of the molecular structure of a novel spider venom toxin, identified as 1-4-guanidinobutoxy-6-hydroxy-1,2,3,4-tetrahydro-b- carboline, and referred to here as PwTx-II. This compound is toxic to insects (LD50Z12G3 hg/mg honeybee), neurotoxic, convulsive and lethal to rats (LD50Z9.75 mg/kg of male Wistar rat). q 2005 Elsevier Ltd. All rights reserved. Keywords: Spider venom; Spider toxin; Natural compound; Alkaloid; Structure determination; Neurotoxicity; Natural product; Spectroscopy 1. Introduction biologically active toxins, which may be grouped into three major classes of compounds according to their Studies of Arthropod defensive chemistries continue to chemical nature: high molecular mass proteins (MwO bring to light novel structures and unanticipated biosyn- 10 kDa), peptides (Mw 3–10 kDa) and low molecular mass thetic capabilities. In the last decade, insecticidal toxins compounds (Mw!1 kDa) (Kawai and Nakajima, 1993). The from Arthropod venoms have been the subject of latter class can be subdivided into other subclasses, considerable emphasis in the literature. Spider venoms according to the chemical nature of these toxins. (Marques generally are constituted of complex mixtures of et al., 2004) The acylpolyamine toxins constitute a large family of neuroblockers of ionotropic glutamate receptors, occurring * Corresponding author. Tel.: C55 19 3526 4163; fax: C55 19 3534 8523. in the venoms of solitary wasps and spiders, acting at the E-mail address: [email protected] (M.S. Palma). level of the neuromuscular junction of Arthropods in 0041-0101/$ - see front matter q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.toxicon.2005.08.005 L.M.M. Cesar et al. / Toxicon 46 (2005) 786–796 787 general, causing paralysis/death (Nakanishi et al., 1990; and its structure has been elucidated through the combined Skinner et al., 1990; Quistad et al., 1993; Palma et al., 1997; use of UV-spectrophotometry, 1H NMR spectroscopy and Palma and Nakajima, 2005). Nucleoside toxins were ESI mass spectrometry. The structural features of 1,4- identified in the venom of the spider Hololena curta; these guanidinobutoxi-6-hydroxy-1,2,3,4-tetrahydro-b-carboline toxins are constituted of mono- and disulphate derivatives of and the study of its insecticidal action may be used, as a guanosine or xantosine, bearing one or two D-fucose units, starting point for the development of new molecules for pest which have the uncommon property of effectively blocking control. kainate receptors, in addition to weakly blocking L-type calcium channels (McCormick et al., 1999). The nucleoside inosine was also demonstrated to be a component of 2. Material and methods Parawixia bistriata venom, which causes paralysis in termites (Rodrigues et al., 2004). The organometallic 2.1. Spider collection, venom extraction and purification diazenaryl compounds are potent insecticidal toxins also identified in the venom of P. bistriata, presenting lethal P. bistriata specimens were collected in Rio Claro, SP, effect even when topically applied on spiders’ preys southeast Brazil. Spiders were sacrificed by freezing at (Marques et al., 2005). K20 8C. Venom glands were removed with surgical micro- The tetrahydrobetacarboline ring, 1,2,3,4-tetrahydro-7H- scissors and the venom was extracted with 1:1 acetonitrile pyrido/3,4-b/indole (THBC) constitutes the basic element of (CH3CN)/ultra pure water. The extract was centrifuged several natural indolyl alkaloids, such as those occurring in through AMICON 3 spin filters (Millipore) at 8000!g some ascidians and plants such as Peganum harmala,or during 15 min at 4 8C and the low molecular mass (LMM) Rauwolfia serpentine (Abramovitch and Spencer, 1964; fraction (!3 kDa) was collected, lyophilized and stored at Szanta´y et al., 1986; Carmona et al., 2000). K10 8C. Tetrahydro-b-carboline compounds are endogenous in The LMM fraction was then solubilized in 5% (v/v) some animals, and found at trace levels in mammalian brain CH3CN in bi-distilled water (containing 0.1% TFA) and (Barker et al., 1981; Johnson et al., 1985). These supposed fractionated in a HPLC system (SHIMADZU, mod. LC- mammalian THBC alkaloids probably arise endogenously 10Advp) equipped with a diode array detector (SHIMADZU, from the condensation of central nervous system indola- mod. SPD-10Avp), using a reversed-phase semi-preparative mines (or their precursor amino acid, L-tryptophan) with an column CapCell Pack-C18 (10!250 mm, 5 mm). Elution aldehyde or a-keto acid via Pictet–Spengler reaction was carried out by linear gradient from 5 to 60% (v/v) (Carmona et al., 2000). These endogenously formed CH3CN in bi-distilled water (containing 0.1% TFA) during alkaloids act on various aspects of neurotransmission 60 min at 30 8C. The UV absorbance was monitored at 220, modulation, and are neurotoxic since they constitute a 254 and 280 nm, at a flow rate of 2.5 mL minK1. family of high affinity ligands of the benzodiazepine (BDZ) receptors which is a sub-type of GABA receptor) 2.2. Mass spectrometry analysis (Robertson, 1980). P. bistriata (Araneidae, Araneae) is a very common Mass spectra were acquired on a triple quadrupole species of social spider in Brazil (Levi, 1992) and its venom (Quatro II) mass spectrometer instrument (Micromass, UK), seems to constitute a rich source of neurotoxins. It was equipped with a standard electrospray probe, adjusted to ca. reported recently that intracerebroventricular (i.c.v.) appli- 5 mL minK1. During all experiments the source temperature cation of the crude venom caused limbic seizures in rats was maintained at 80 8C and the needle voltage at 3.6 kV, (Rodrigues et al., 2001); in addition to this, an isolated applying a drying gas flow (nitrogen) of 200 L hK1 and a fraction of this venom (not structurally characterized) nebulizer gas flow (nitrogen) of 20 L hK1.Themass inhibited the uptaking of GABA in rat cortical sinaptos- spectrometer was calibrated with intact horse heart somes (Rodrigues et al., 2002). P. bistriata uses tetrahydro- myoglobin and its typical cone-voltage induced fragments. b-carboline compounds as part of its chemical weaponry to The cone sample to skimmer lens voltage, controlling the kill/paralyse the Arthropod preys (Marques et al., 2005). ion transfer to the mass analyzer, was maintained at 30 V. These molecules are natural analogues of trypargine [1-(30- About 50 pmol of each sample was injected into electro- guanidinopropyl)-1,2,3,4-tetrahydro-b-carboline]; an alka- spray transport solvent. The ESI spectra were obtained in the loid compound previously isolated from the skin of the continuous acquisition mode, scanning from m/z 100 to African frog Kassina senegalensis (Akizawa et al., 1982). 2000 with a scan time of 5 s. Recently, an indoleyl alkaloid compound was reported in the venom of this spider and characterized as a potent 2.3. MS/MS spectrometry experiments insecticide toxin (Cesar et al., 2005). A novel alkaloid toxin has been now identified in the crude venom of the Typical conditions were: a capillary voltage of 3 kV, a K3 P. bistriata; it was isolated from acetonitrile (CH3CN) cone voltage of 30 V, collision gas pressure of 3.5!10 extracts of the crude venom by chromatographic techniques, mbar and a desolvation gas temperature of 80 8C. In these 788 L.M.M. Cesar et al. / Toxicon 46 (2005) 786–796 experiments Q1 was used to select the parent ion and was not microsyringe (10 mL). The insects were kept in a Petri dish scanned. The ion of interest was individually selected in Q1 up to 4 h in the presence of candy (food) and water supply. and structurally characterized by collision-induced dis- During this period the toxicity effects and/or the lethal sociation (CID). It was subjected to about 25 eV collision action of the new toxins were observed. Control exper- energy and 5!10K3 mbar collision gas pressure (argon) in iments were performed by injecting the physiological Q2. The CID fragments were analyzed by scanning Q3. solution into the insect pronotum. Toxicity levels were calculated according to the Probit method (Chou and Chou, 2.4. Nuclear magnetic resonance experiments 1987) and expressed as 50% lethal doses (LD50). Results are expressed as meansGS.D. of five experiments. Differences The 1H NMR spectrum was recorded at 25 8Cona between the two extracts (reconstituted and non-reconsti- Varian INOVA 500 spectrometer, operating at 499.88 MHz tuted) were evaluated with Students’ t-test.
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